Abstract Evolutionary transitions from hermaphroditism to dioecy have been frequent in flowering plants, but recent analysis indicates that reversions from dioecy to hermaphroditism have also been common. Here, we use experimental evolution to expose a mechanism for such reversions. We removed males from dioecious populations of the wind-pollinated plant Mercurialis annua and allowed natural selection to act on the remaining females that varied in their propensity for the occasional production of male flowers; such ‘leaky’ sex expression is common in both males and females of dioecious plants. Over only four generations, females evolved a 23-fold increase in average male-flower production. The phenotypic masculinization of females was also sufficient to render them effective at siring progeny in the presence of males. Our study illustrates the rapid dissolution of dioecy and the evolution of functional hermaphroditism under conditions that may frequently occur during periods of low population density, repeated colonization, or range expansion. It thereby experimentally validates a mechanism for a major transition in plant sexual systems..